Basin-scale distributions of stable nitrogen isotopes in the subtropical North Atlantic Ocean: Contribution of diazotroph nitrogen to particulate organic matter and mesozooplankton

Deep-Sea Research Part I: Oceanographic Research Papers

Volumn 58, Issue 5, 2011, Pages 615-625

  Landrum, Jason P ^a   Altabet, Mark A ^b   Montoya, Joseph P ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF MASSACHUSETTS DARTMOUTH   (United States)

Author keywords

Diazotrophs; Mesozooplankton; Nitrogen; North Atlantic; Stable isotopes

Indexed keywords

BIOGEOCHEMICAL CYCLE; DIAZOTROPHS; FOOD WEBS; KEY COMPONENT; MESOZOOPLANKTON; NATURAL ABUNDANCE; NORTH ATLANTIC; NORTH ATLANTIC OCEAN; PARTICULATE ORGANIC MATTERS; PRIMARY PRODUCTION; SCALE DISTRIBUTIONS; SECONDARY PRODUCTION; SPATIAL SCALE; SPATIAL TRENDS; STABLE ISOTOPES; STABLE NITROGEN ISOTOPE; SUSPENDED PARTICLES; TEMPORAL VARIATION; TIME-SCALES; WATER COLUMNS; WESTERN ATLANTIC;

BIOGEOCHEMISTRY; BIOLOGICAL MATERIALS; ECOLOGY; ISOTOPES; NITROGEN; PRODUCTION;

OCEANOGRAPHY;

BIOGEOCHEMICAL CYCLE; FOOD WEB; NITROGEN FIXATION; NITROGEN ISOTOPE; PARTICULATE ORGANIC MATTER; PRIMARY PRODUCTION; SECONDARY PRODUCTION; STABLE ISOTOPE; ZOOPLANKTON;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTH);

EID: 79955484650     PISSN: 09670637     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dsr.2011.01.012     Document Type: Article

References (79)

1. Aberle N., Malzahn A.M. Interspecific and nutrient-dependent variations in stable isotope fractionation: experimental studies simulating pelagic multitrophic systems. Oecologia 2007, 154(2):291-303. 10.1007/s00442-007-0829-5.
2. Adams T.S., Sterner R.W. The effect of dietary nitrogen content on trophic level N-15 enrichment. Limnology and Oceanography 2000, 45(3):601-607.
3. Altabet M.A., Deuser W.G., Honjo S., Stienen C. Seasonal and depth-related changes in the source of sinking particles in the North Atlantic. Nature 1991, 354(6349):136-139.
4. Baker A.R., Jickells T.D., Biswas K.F., Weston K., French M. Nutrients in atmospheric aerosol particles along the atlantic meridional transect. Deep-Sea Research Part II-Topical Studies in Oceanography 2006, 53(14-16):1706-1719.
5. Berman-Frank I., Bidle K.D., Haramaty L., Falkowski P.G. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnology and Oceanography 2004, 49(4):997-1005.
6. Bourbonnais A., Lehmann M.F., Waniek J.J., Schulz-Bull D.E. Nitrate isotope anomalies reflect N2-fixation in the Azores front region (subtropical NE atlantic). Journal of Geophysical Research-Oceans 2009, 114. 10.1029/2007JC004617.
7. Brandes J.A., Devol A.H. A global marine-fixed nitrogen isotopic budget: implications for holocene nitrogen cycling. Global Biogeochemical Cycles 2002, 16(4). 10.1029/2001GB001856.
8. Brandes J.A., Devol A.H., Deutsch C. New developments in the marine nitrogen cycle. Chemical Reviews 2007, 107(2):577-589.
9. Bullard S.B., Hay M.E. Palatability of marine macro-holoplankton: nematocysts, nutritional quality, and chemistry as defenses against consumers. Limnology and Oceanography 2002, 47(5):1456-1467.
10. Capone D.G., Burns J.A., Montoya J.P., Subramaniam A., Mahaffey C., Gunderson T., Michaels A.F., Carpenter E.J. Nitrogen fixation by Trichodesmium spp.: an important source of new nitrogen to the tropical and subtropical north atlantic ocean. Global Biogeochemical Cycles 2005, 19(2). 10.1029/2004GB002331.
11. Capone D.G., Subramaniam A., Montoya J.P., Voss M., Humborg C., Johansen A.M., Siefert R.L., Carpenter E.J. An extensive bloom of the N2-fixing cyanobacterium Trichodesmium erythraeum in the central Arabian Sea. Marine Ecology-Progress Series 1998, 172:281-292.
12. Capone D.G., Zehr J.P., Paerl H.W., Bergman B., Carpenter E.J. Trichodesmium, a globally significant marine cyanobacterium. Science 1997, 276(5316):1221-1229.
13. Carpenter E.J., Montoya J.P., Burns J., Mulholland M.R., Subramaniam A., Capone D.G. Extensive bloom of a N2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean. Marine Ecology-Progress Series 1999, 185:273-283.
14. Carpenter E.J., Subramaniam A., Capone D.G. Biomass and primary productivity of the cyanobacterium Trichodesmium spp. in the tropical north Atlantic ocean. Deep-Sea Research Part I-Oceanographic Research Papers 2004, 51(2):173-203.
15. Checkley D.M., Miller C.A. Nitrogen isotope fractionation by oceanic zooplankton. Deep-Sea Research Part A-Oceanographic Research Papers 1989, 36(10):1449-1456.
16. Church M.J., Jenkins B.D., Karl D.M., Zehr J.P. Vertical distributions of nitrogen-fixing phylotypes at Stn ALOHA in the oligotrophic north pacific ocean. Aquatic Microbial Ecology 2005, 38(1):3-14.
17. Clark D.R., Rees A.P., Joint I. Ammonium regeneration and nitrification rates in the oligotrophic atlantic ocean: implications for new production estimates. Limnology and Oceanography 2008, 53(1):52-62.
18. Cornell S.E., Jickells T.D., Thornton C.A. Atmospheric inputs of dissolved organic nitrogen to the oceans. Nature 1995, 376(6537):243-246.
19. Davis C.S., McGillicuddy D.J. Transatlantic abundance of the N2-fixing colonial cyanobacterium Trichodesmium. Science 2006, 312(5779):1517-1520.
20. Deniro M.J., Epstein S. Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 1981, 45(3):341-351.
21. Doi H., Chang K.-H., Nakano S-i. Nitrogen and carbon isotope fractionations of zooplankton consumers in ponds: potential effects of seston C:N stoichiometry. Marine and Freshwater Research 2011, 62:66-71. 10.1071/MF10090.
22. Dore J.E., Brum J.R., Tupas L.M., Karl D.M. Seasonal and interannual variability in sources of nitrogen supporting export in the oligotrophic subtropical north pacific ocean. Limnology and Oceanography 2002, 47(6):1595-1607.
23. Duarte C.M., Dachs J., Llabres M., Alonso-Laita P., Gasol J.M., Tovar-Sanchez A., Sanudo-Wilhemy S., Agusti S. Aerosol inputs enhance new production in the subtropical northeast atlantic. Journal of Geophysical Research-Biogeosciences 2006, 111(G4). 10.1029/2005JG000140.
24. Duce R.A., LaRoche J., Altieri K., Arrigo K.R., Baker A.R., Capone D.G., Cornell S., Dentener F., Galloway J., Ganeshram R.S., Geider R.J., Jickells T., Kuypers M.M., Langlois R., Liss P.S., Liu S.M., Middelburg J.J., Moore C.M., Nickovic S., Oschlies A., Pedersen T., Prospero J., Schlitzer R., Seitzinger S., Sorensen L.L., Uematsu M., Ulloa O., Voss M., Ward B., Zamora L. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 2008, 320(5878):893-897.
25. Dugdale R.C., Goering J.J. Uptake of new and regenerated forms of nitrogen in primary productivity. Limnology and Oceanography 1967, 12(2):196-206.
26. Eppley R.W., Peterson B.J. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 1979, 282(5740):677-680.
27. Falcon L.I., Carpenter E.J., Cipriano F., Bergman B., Capone D.G. N2-fixation by unicellular bacterioplankton from the atlantic and pacific oceans: phylogeny and in situ rates. Applied and Environmental Microbiology 2004, 70(2):765-770.
28. Foster R.A., Subramaniam A., Mahaffey C., Carpenter E.J., Capone D.G., Zehr J.P. Influence of the Amazon River plume on distributions of free-living and symbiotic cyanobacteria in the western tropical north atlantic ocean. Limnology and Oceanography 2007, 52(2):517-532.
29. Fry B., Quinones R.B. Biomass spectra and stable isotope indicators of trophic level in zooplankton of the northwest atlantic. Marine Ecology-Progress Series 1994, 112(1-2):201-204.
30. Galloway J.N., Townsend A.R., Erisman J.W., Bekunda M., Cai Z.C., Freney J.R., Martinelli L.A., Seitzinger S.P., Sutton M.A. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 2008, 320(5878):889-892.
31. Graziano L.M., Geider R.J., Li W.K.W., Olaizola M. Nitrogen limitation of north atlantic phytoplankton: analysis of physiological condition in nutrient enrichment experiments. Aquatic Microbial Ecology 1996, 11(1):53-64.
32. Gruber N., Sarmiento J.L. Global patterns of marine nitrogen fixation and denitrification. Global Biogeochemical Cycles 1997, 11(2):235-266. 10.1029/97GB00077.
33. Hawser S.P., Carpenter E.J., Codd G.A., Capone D.G. A neurotoxic factor associated with the bloom-forming cyanobacterium Trichodesmium. Toxicon 1991, 29(3):277-278.
34. Hawser S.P., Oneil J.M., Roman M.R., Codd G.A. Toxicity of blooms of the cyanobacterium-Trichodesmium to zooplankton. Journal of Applied Phycology 1992, 4(1):79-86.
35. Hewson I., Govil S.R., Capone D.G., Carpenter E.J., Fuhrman J.A. Evidence of Trichodesmium viral lysis and potential significance for biogeochemical cycling in the oligotrophic ocean. Aquatic Microbial Ecology 2004, 36(1):1-8.
36. Holl C.M., Villareal T.A., Payne C.D., Clayton T.D., Hart C., Montoya J.P. Trichodesmium in the western Gulf of Mexico: 15N2-fixation and natural abundance stable isotope evidence. Limnology and Oceanography 2007, 52(5):2249-2259.
37. Karl D.M., Letelier R.M. Nitrogen fixation-enhanced carbon sequestration in low nitrate, low chlorophyll seascapes. Marine Ecology-Progress Series 2008, 364:257-268.
38. Knapp A.N., DiFiore P.J., Deutsch C., Sigman D.M., Lipschultz F. Nitrate isotopic composition between Bermuda and Puerto Rico: implications for N2 fixation in the atlantic ocean. Global Biogeochemical Cycles 2008, 22(3). 10.1029/2007GB003107.
39. Knapp A.N., Sigman D.M., Lipschultz F. N isotopic composition of dissolved organic nitrogen and nitrate at the Bermuda atlantic time-series study site. Global Biogeochemical Cycles 2005, 19(1). 10.1029/2004GB002320.
40. Koppelmann R., Bottger-Schnack R., Mobius J., Weikert H. Trophic relationships of zooplankton in the eastern Mediterranean based on stable isotope measurements. Journal of Plankton Research 2009, 31(6):669-686. 10.1093/plankt/fbp013.
41. Langlois R.J., Hummer D., LaRoche J. Abundances and distributions of the dominant nifH phylotypes in the northern atlantic ocean. Applied and Environmental Microbiology 2008, 74(6):1922-1931.
42. LaRoche J., Breitbarth E. Importance of the diazotrophs as a source of new nitrogen in the ocean. Journal of Sea Research 2005, 53(1-2):67-91.
43. Lehmann M.F., Bernasconi S.M., Barbieri A., McKenzie J.A. Preservation of organic matter and alteration of its carbon and nitrogen isotope composition during simulated and in situ early sedimentary diagenesis. Geochimica et Cosmochimica Acta 2002, 66(20):3573-3584.
44. Letelier R.M., Karl D.M. Role of Trichodesmium spp. in the productivity of the subtropical north pacific ocean. Marine Ecology-Progress Series 1996, 133(1-3):263-273.
45. Letelier R.M., Karl D.M. Trichodesmium spp. physiology and nutrient fluxes in the north pacific subtropical gyre. Aquatic Microbial Ecology 1998, 15(3):265-276.
46. Lewis M.R., Harrison W.G., Oakey N.S., Hebert D., Platt T. Vertical nitrate fluxes in the oligotrophic ocean. Science 1986, 234(4778):870-873.
47. Macko S.A., Engel M.H., Qian Y.R. Early diagenesis and organic matter preservation-a molecular stable carbon isotope perspective. Chemical Geology 1994, 114(3-4):365-379.
48. Mahaffey C., Michaels A.F., Capone D.G. The conundrum of marine N2-fixation. American Journal of Science 2005, 305(6-8):546-595.
49. Mahaffey C., Williams R.G., Wolff G.A., Anderson W.T. Physical supply of nitrogen to phytoplankton in the atlantic ocean. Global Biogeochemical Cycles 2004, 18(1). 10.1029/2003GB002129.
50. Mariotti A., Germon J.C., Hubert P., Kaiser P., Letolle R., Tardieux A., Tardieux P. Experimental determination of nitrogen kinetic isotope fractionation - Some principles - Illustration for the denitrification and nitrification processes. Plant and Soil 1981, 62(3):413-430.
51. Martins R., Fernandez N., Beiras R., Vasconcelos V. Toxicity assessment of crude and partially purified extracts of marine Synechocystis and Synechococcus cyanobacterial strains in marine invertebrates. Toxicon 2007, 50(6):791-799.
52. McClelland J.W., Montoya J.P. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 2002, 83(8):2173-2180.
53. McGillicuddy D.J., Robinson A.R., Siegel D.A., Jannasch H.W., Johnson R., Dickeys T., McNeil J., Michaels A.F., Knap A.H. Influence of mesoscale eddies on new production in the Sargasso Sea. Nature 1998, 394(6690):263-266.
54. Meador T.B., Aluwihare L.I., Mahaffey C. Isotopic heterogeneity and cycling of organic nitrogen in the oligotrophic ocean. Limnology and Oceanography 2007, 52(3):934-947.
55. Minagawa M., Wada E. Stepwise enrichment of 15N along food-chains-further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 1984, 48(5):1135-1140.
56. Mino Y., Saino T., Suzuki K., Maranon E. Isotopic composition of suspended particulate nitrogen (δ15Nsus) in surface waters of the atlantic ocean from 50° N to 50° S. Global Biogeochemical Cycles 2002, 16(4). 10.1029/2001GB001635.
57. Moisander P.H., Beinart R.A., Hewson I., White A.E., Johnson K.S., Carlson C.A., Montoya J.P., Zehr J.P. Unicellular cyanobacterial distributions broaden the oceanic N2-fixation domain. Science 2010, 327(5972):1512-1514.
58. Montoya J.P. Nitrogen stable isotopes in marine environments. Nitrogen in the Marine Environment 2008, 1277-1302. Academic Press. D.G. Capone, E.J. Carpenter, M.R. Mulholland, D.A. Bronk (Eds.).
59. Montoya J.P., Carpenter E.J., Capone D.G. Nitrogen fixation and nitrogen isotope abundances in zooplankton of the oligotrophic north atlantic. Limnology and Oceanography 2002, 47(6):1617-1628.
60. Montoya J.P., Holl C.M., Zehr J.P., Hansen A., Villareal T.A., Capone D.G. High rates of N2-fixation by unicellular diazotrophs in the oligotrophic pacific ocean. Nature 2004, 430(7003):1027-1031.
61. Montoya J.P., Voss M., Capone D.G. Spatial variation in N2-fixation rate and diazotroph activity in the tropical atlantic. Biogeosciences 2007, 4(3):369-376. 10.5194/bg-4-369-2007.
62. Montoya J.P., Wiebe P.H., McCarthy J.J. Natural abundance of 15N in particulate nitrogen and zooplankton in the Gulf-Stream region and warm-core ring 86a. Deep-Sea Research Part A-Oceanographic Research Papers 1992, 39(1A):S363-S392.
63. Moore C.M., Mills M.M., Langlois R., Milne A., Achterberg E.P., La Roche J., Geider R.J. Relative influence of nitrogen and phosphorus availability on phytoplankton physiology and productivity in the oligotrophic sub-tropical north atlantic ocean. Limnology and Oceanography 2008, 53(1):291-305.
64. Mulholland M.R. The fate of nitrogen fixed by diazotrophs in the ocean. Biogeosciences 2007, 4(1):37-51. 10.5194/bg-4-37-2007.
65. Mulholland M.R., Bernhardt P.W., Heil C.A., Bronk D.A., O'Neil J.M. Nitrogen fixation and release of fixed nitrogen by Trichodesmium spp. in the Gulf of Mexico. Limnology and Oceanography 2006, 51(4):1762-1776.
66. Mulholland M.R., Bronk D.A., Capone D.G. Dinitrogen fixation and release of ammonium and dissolved organic nitrogen by Trichodesmium IMS101. Aquatic Microbial Ecology 2004, 37(1):85-94.
67. O'Neil J.M. The colonial cyanobacterium Trichodesmium as a physical and nutritional substrate for the harpacticoid copepod Macrosetella gracilis. Journal of Plankton Research 1998, 20(1):43-59.
68. O'Neil J.M., Metzler P.M., Glibert P.M. Ingestion of 15N2-labelled Trichodesmium spp. and ammonium regeneration by the harpacticoid copepod Macrosetella gracilis. Marine Biology 1996, 125(1):89-96.
69. Post D.M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 2002, 83(3):703-718.
70. Reynolds S.E., Mather R.L., Wolff G.A., Williams R.G., Landolfi A., Sanders R., Woodward E.M.S. How widespread and important is N2-fixation in the north atlantic ocean?. Global Biogeochemical Cycles 2007, 21(4). 10.1029/2006GB002886.
71. Ryther J.H., Dunstan W.M. Nitrogen, phosphorus, and eutrophication in coastal marine environment. Science 1971, 171(3975):1008-1013.
72. Sanudo-Wilhelmy S.A., Kustka A.B., Gobler C.J., Hutchins D.A., Yang M., Lwiza K., Burns J., Capone D.G., Raven J.A., Carpenter E.J. Phosphorus limitation of nitrogen fixation by Trichodesmium in the central atlantic ocean. Nature 2001, 411(6833):66-69.
73. Schlitzer, R., 2008. Ocean Data View. 〈〉. http://odv.awi.de.
74. Sheridan C.C., Steinberg D.K., Kling G.W. The microbial and metazoan community associated with colonies of Trichodesmium spp.: a quantitative survey. Journal of Plankton Research 2002, 24(9):913-922.
75. 13;C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 2001, 46(8):2061-2066.
76. Waser N.A., Harrison W.G., Head E.J.H., Nielson B., Lutz V.A., Calvert S.E. Geographic variations in the nitrogen isotope composition of surface particulate nitrogen and new production across the north atlantic ocean. Deep-Sea Research Part I-Oceanographic Research Papers 2000, 47(7):1207-1226.
77. West J.B., Bowen G.J., Cerling T.E., Ehleringer J.R. Stable isotopes as one of nature's ecological recorders. Trends in Ecology & Evolution 2006, 21(7):408-414.
78. Westberry T.K., Siegel D.A. Spatial and temporal distribution of Trichodesmium blooms in the world's oceans. Global Biogeochemical Cycles 2006, 20(4). 10.1029/2005GB002673.
79. Zehr J.P., Montoya J.P., Jenkins B.D., Hewson I., Mondragon E., Short C.M., Church M.J., Hansen A., Karl D.M. Experiments linking nitrogenase gene expression to nitrogen fixation in the north pacific subtropical gyre. Limnology and Oceanography 2007, 52(1):169-183.